Cold adaptation drives population genomic divergence in the ecological specialist,Drosophila montana

Abstract

3 6 9 12 15 ABSTRACT Detecting signatures of ecological adaptation in comparative genomics is challenging, but analysing population samples with characterised geographic distributions, such as clinal variation, can help identify genes showing covariation with important ecological variation. Here we analysed patterns of geographic variation in the cold-adapted species Drosophila montana across phenotypes, genotypes and environmental conditions and searched for signatures of cold adaptation inpopulations' genomic divergence. We first derived the climatic variables associated with the geographic distribution of 24 populations across two continents to trace the whole scale of environmental variation experienced by the species, and measure variation in the cold tolerance of the flies of six populations from different geographic contexts. We then performed pooled whole genome sequencing of these six populations, and used Bayesian methods to identify SNPs where genetic differentiation is associated with both climatic variables and the population phenotypic measurements. The top candidate SNPs were enriched on the X and 4 th chromosomes, and they also lie near genes implicated in other studies of cold tolerance and population divergence in this species and its close relatives. We conclude that ecological adaptation has contributed to the divergence of D. montana populations throughout the genome and in particular on the X and 4 th chromosomes, which also showed highest interpopulation F st . This study demonstrates that ecological selection can drive genomic divergence at different scales, from candidate genes to chromosome-wide effects.

Multiple paths to cold tolerance: the role of environmental cues, morphological traits and the circadian clock genevrille

“…Latitudinal variation in CCRT, but not in CTmin, has also been observed in two widespread ant species, Myrmica rubra and Myrmica ruginodis [29]. Although it is possible that the low variation in cold tolerance in our study is a consequence of relatively low number of studied strains or populations, a recent study found similar trends when using mass-bred D. montana populations for a limited number of places from North America [89].…”

“…The candidate gene D. virilis species group shows several distinct features in their circadian clock system compared to D. melanogaster, which has enabled their adaptation in high-latitudes [72][73][74]. Interestingly, vrille was the only core circadian clock gene that was found to show both population-level differentiation in clinal cold tolerance study [89] as well as expression level differences when cold-acclimated and non-acclimated D. montana flies were compared [77]. This gene was also one of the differentially expressed genes in our earlier microarray study investigating cold tolerance of D. montana and D. virilis [65].…”

Nanda-Hamner Curves Show Huge Latitudinal Variation but No Circadian Components in Drosophila Montana Photoperiodism

“…Insect species with a wide distribution offer a great opportunity to trace latitudinal variation in traits that are important in reproduction and stress tolerances, and particularly in the contribution of circadian clock(s) and/or PPTM in their regulation. Our study species, D. montana , shows steep latitudinal clines in CDL and its temperature-sensitivity ( Tyukmaeva et al, 2020 ), as well as in the flies’ basal cold tolerance ( Wiberg et al, 2020 ). In the present study, variation in the diapause proportions of D. montana cline strains, and the control and selection lines, in extra long and short photoperiods revealed many interesting aspects of PPTM related to our study questions.…”

Divergence and introgression among the virilis group of Drosophila

“…Also morphological differences, particularly in body pigmentation, have been documented in this group, though the evolutionary processes underpinning pigmentation differences is not yet well understood (Wittkopp et al 2002, Wittkopp et al 2002; Kulikov et al 2004; Bubliy et al 2007; Ahmed-Braimah and Sweigart 2015; Lamb et al 2020). Several species of the virilis group, especially those of the montana phylad, persist in extreme cold environments, and show high cold acclimation and diapause which may contribute to genomic divergence (Vesala et al 2012; Parker et al 2015, 2016; Salminen et al 2015; Tyukmaeva et al 2015; Wiberg et al 2021). Fixed and polymorphic chromosomal inversions have been reported within the group and may be driven by the activity and expansion of transposable elements, giving rise to regions of high differentiation between species and populations (Evgen’ev et al 2000; Fonseca et al 2013; Reis et al 2018).…”